Gedächtnisprozesse im medialen Temporallappen: Jenseits des Langzeitgedächtnisses

Zusammenfassung

Einleitung: Gedächtnis ist kein einheitlicher Prozess, sondern besteht aus verschiedenen Subsystemen, die jeweils unterschiedliche neuronale Korrelate besitzen. Während seit längerem bekannt ist, dass der mediale Temporallappen (MTL) eine zentrale Rolle für die Einspeicherung und den Abruf deklarativer Gedächtnisinhalte spielt, wurde aufgrund früherer Studien angenommen, dass diese Hirnregion für Arbeitsgedächtnis eher irrelevant ist. Auch über die neuronalen Prozesse, die beim Menschen während der Konsolidierung von Langzeitgedächtnis-Inhalten im MTL auftreten, ist bisher wenig bekannt.

Methodik und Material: In diesem Übersichtsartikel werden mehrere Studien zur Rolle des MTL für Arbeitsgedächtnis und Langzeitgedächtnis-Konsolidierung zusammengefasst, die in der Klinik für Epileptologie der Universität Bonn während der Jahre 2006–2008 durchgeführt wurden. Methodisch basieren diese Studien einerseits auf intrakraniellen EEG-Ableitungen an Epilepsiepatienten, andererseits auf Messungen mittels funktioneller Magnetresonanztomografie an gesunden Probanden.

Ergebnisse und Diskussion: Anders als lange angenommen zeigte sich, dass der MTL durchaus eine Rolle für die Aufrechterhaltung von Inhalten im Arbeitsgedächtnis spielt. Dies scheint insbesondere dann der Fall zu sein, wenn mehrere Inhalte gleichzeitig gemerkt werden müssen. Studien zur Langzeitgedächtnis-Konsolidierung zeigten, dass hochfrequente Populationsentladungen (sogenannte „ripples”) während des Schlafes im MTL prädiktiv für den Erfolg der Langzeitgedächtnis-Konsolidierung sind. Diese Ergebnisse weisen darauf hin, dass die bisher angenommene exklusive Funktion des MTL für die Einspeicherung und den Abruf deklarativer Gedächtnisinhalte revidiert werden muss.

Abstract

Introduction: Memory is not a unitary process, but can be divided into multiple subsystems with distinct neuronal correlates. While it is well known that the medial temporal lobe (MTL) plays a crucial role in encoding into and retrieval from long-term memory, its relevance for other memory processes is currently under debate. Traditionally, it has been assumed that the MTL only plays a minor role during maintenance of items in working memory. The neural processes in the MTL during consolidation of items in long-term memory still remain to be investigated in humans.

Materials and Methos: In this review, we summarise several studies on the role of the MTL for working memory and long-term memory consolidation, which have been conducted at the Department of Epileptology, University of Bonn, during the years 2006–2008. These studies used intracranial EEG recordings in epilepsy patients as well as functional magnetic resonance imaging in healthy control subjects.

Results and Discussion: Contrary to traditional assumptions, these studies show that the MTL does play a role for maintenance of items in working memory. This appears to be particularly the case when multiple items need to be processed simultaneously. Studies on long-term memory consolidation showed that the incidence of high-frequency population bursts (“ripples”) within the MTL during sleep is predictive for the success of consolidation. These results suggest that the hypothesis of an exclusive function of the MTL for encoding into and retrieval from long-term memory needs to be revised.

Schlüsselwörter

Arbeitsgedächtnis - Gedächtnis-Konsolidierung - intrakranielle EEG - funktionelle Magnetresonanztomografie - Gedächtnissysteme

Key words

working memory - memory consolidation - intracranial EEG - functional MRI - memory systems

Literatur

• 1 Ebbinghaus H. Über das Gedächtnis. Leipzig, Verlag von Duncker & Humblot; 1885
• 2 Atkinson RC, Shiffrin RM. Human memory : A proposed system and its control processes. In:, Spence KW, Spence JT, Hrsg. The psychology of learning and motivation, Vol. 2 (pp. 89–195). New York: Academic Press; 1968
• 3 Baddeley A, Hirch G. Working memory. In:, Bower GH, Hrsg. The psychology of learning and motivation, Vol. 8 (pp. 47–89). New York: Academic Press.; 1974
• 4 Baddeley A. Working memory: looking back and looking forward.  Nat Rev Neurosci. 2003;  4 829-839
• 5 Gazzaniga MS, Ivry RB, Mangun GR. Cognitive neuroscience: the biology of the mind. Second edition. New York/London: Norton and Company; 2002: S313-S315
• 6 Buzsaki G. Two-stage model of memory trace formation: a role for ‘‘noisy’’ brain states.  Neuroscience. 1989;  31 551-570
• 7 Hasselmo ME. Neuromodulation: acetylcholine and memory consolidation.  Trends Cogn Sci. 1999;  3 351-359
• 8 Wiltgen BJ, Brown RA, Talton LE. et al . New circuits for old memories: the role of the neocortex in consolidation.  Neuron. 2004;  44 101-108
• 9 Stickgold R, Hobson JA, Fosse R. et al . Sleep, learning, and dreams: off-line memory reprocessing.  Science. 2001;  294 1052-1057
• 10 Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions.  J Neurol Neurosurg Psychiatry. 1957;  20 11-21
• 11 Penfield W, Milner B. Memory deficit produced by bilateral lesions in the hippocampal zone.  AMA Arch Neurol Psychiatry. 1958;  79 475-497
• 12 Gabrieli JD, Milberg W, Keane MM. et al . Intact priming of patterns despite impaired memory.  Neuropsychologia. 1990;  28 417-427
• 13 Cave CB, Squire LR. Intact verbal and nonverbal short-term memory following damage to the human hippocampus.  Hippocampus. 1992;  2 151-163
• 14 Aggleton JP, Shaw C, Gaffan EA. The performance of postencephalitic amnesic subjects on two behavioural tests of memory: concurrent discrimination learning and delayed matching-to-sample.  Cortex. 1992;  28 359-372
• 15 Hannula DE, Tranel D, Cohen NJ. The long and the short of it: relational memory impairments in amnesia, even at short lags.  J Neurosci. 2006;  262 8352-8359
• 16 Olson IR, Page K, Moore KS. et al . Working memory for conjunctions relies on the medial temporal lobe.  J Neurosci. 2006;  26 4596-4601
• 17 Piekema C, Kessels RP, Mars RB. et al . The right hippocampus participates in short-term memory maintenance of object-location associations.  Neuroimage. 2006;  33 374-382
• 18 Young BJ, Otto T, Fox GD. et al . Memory representation within the parahippocampal region.  J Neurosci. 1997;  17 5183-5195
• 19 Logothetis NK. What we can do and what we cannot do with fMRI.  Nature. 2008;  453 869-878
• 20 Axmacher N, Haupt S, Fernández G. et al . The role of sleep in declarative memory consolidation – direct evidence by intracranial EEG.  Cereb Cortex. 2008;  18 500-507
• 21 Gais S, Born J. Declarative memory consolidation: mechanisms acting during human sleep.  Learn Mem. 2004;  11 679-685
• 22 Stickgold R. Sleep-dependent memory consolidation.  Nature. 2005;  437 1272-1278
• 23 Gais S, Lucas B, Born J. Sleep after learning aids memory recall.  Learn Mem. 2006;  13 259-262
• 24 Buzsaki G. Hippocampal sharp waves: their origin and significance.  Brain Res. 1986;  398 242-252
• 25 Bragin A, Jando G, Nadasdy Z. et al . Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat.  J Neurosci. 1995;  15 47-60
• 26 O’Neill J, Senior T, Csicsvari J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior.  Neuron. 2006;  49 (1) 143-155
• 27 Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state.  Nature. 2006;  440 (7084) 680-683
• 28 Peigneux P, Orban P, Balteau E. et al . Offline persistence of memory-related cerebral activity during active wakefulness.  PLoS Biol. 2006;  4 e100
• 29 Tononi G, Cirelli C. Sleep function and synaptic homeostasis.  Sleep Med Rev. 2006;  10 49-62
• 30 Yoo SS, Hu PT, Gujar N. et al . A deficit in the ability to form new human memories without sleep.  Nat Neurosci. 2007;  10 385-392
• 31 Nadel L, Moscovitch M. The hippocampal complex and long-term memory revisited.  Trends Cogn Sci. 2001;  5 228-230
• 32 Axmacher N, Elger CE, Fell J. Ripples in the medial temporal lobe are relevant for human memory consolidation.  Brain. Jul 2008;  131 (Pt 7) 1806-1817
• 33 Sirota A, Csicsvari J, Buhl D. et al . Communication between neocortex and hippocampus during sleep in rodents.  Proc Natl Acad Sci USA. 2003;  100 2065-2069
• 34 Mölle M, Yeshenko O, Marshall L. et al . Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep.  J Neurophysiol. 2006;  96 62-70
• 35 Gais S, Mölle M, Helms K. et al . Learning-dependent increases in sleep spindle density.  J Neurosci. 2002;  22 6830-6834
• 36 Bragin A, Engel Jr J, Wilson CL. et al . High-frequency oscillations in human brain.  Hippocampus. 1999;  9 137-142
• 37 Axmacher N, Mormann F, Fernández G. et al . Sustained neural activity patterns during working memory in the human medial temporal lobe.  J Neurosci. 2007;  27 (29) 7807-7816
• 38 Birbaumer N, Elbert T, Canavan AGM. et al . Slow potentials of the cerebral cortex and behaviour.  Physiol Rev. 1990;  70 1-41
• 39 Rösler F, Heil M, Röder B. Slow negative brain potentials as reflections of specific modular resources of cognition.  Biol Psychol. 1997;  45 109-141
• 40 Speckmann EJ, Elger CE. Introduction to the neurophysiological basis of the EEG and DC potentials. Baltimore: Lippincott, Williams and Wilkins; 1999
• 41 Daubechies I. The wavelet transform, time-frequency localization and signal analysis.  IEEE Trans Inform Theory. 1990;  36 961-1005
• 42 Reddy L, Kanwisher N. Coding of visual objects in the ventral stream.  Curr Opin Neurobiol. 2006;  16 408-414
• 43 Jensen O, Lisman JE. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer.  Trends Neurosci. 2005;  28 67-72
• 44 Fiebach CJ, Rissman J, D’Esposito M. Modulation of inferotemporal cortex activation during verbal working memory maintenance.  Neuron. 2006;  51 251-261
• 45 Rissman J, Gazzaley A, D’Esposito M. Dynamic Adjustments in Prefrontal, Hippocampal, and Inferior Temporal Interactions with Increasing Visual Working Memory Load.  Cereb Cortex. 2008;  18 1618-1629
• 46 Axmacher N, Schmitz DP, Wagner T. et al . Interactions between medial temporal lobe, prefrontal cortex, and inferior temporal regions during visual working memory: A combined intracranial EEG and functional magnetic resonance imaging study.  J Neurosci. Jul 16 2008;  28 (29) 7304-7312
• 47 Lachaux JP, Rodriguez E, Martinerie J. et al . Measuring phase synchrony in brain signals.  Hum Brain Mapp. 1999;  8 194-208
• 48 Fell J, Klaver P, Lehnertz K. et al . Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling.  Nat Neurosci. 2001;  4 1259-1264
• 49 Tallon-Baudry C, Bertrand O, Fischer C. Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance.  J Neurosci. 2001;  21 RC177
• 50 Rosenblum MG, Pikovsky AS. Detecting direction of coupling in interacting oscillators.  Phys Rev E. 2001;  64 045202(R)
• 51 Schon K, Hasselmo ME, Lopresti ML. et al . Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: a functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task.  J Neurosci. 2004;  24 11088-11097
• 52 Ranganath C, Cohen MX, Brozinsky CJ. Working memory maintenance contributes to long-term memory formation: neural and behavioral evidence.  J Cogn Neurosi. 2005;  17 994-1010
• 53 Axmacher N, Schmitz DP, Weinreich I. et al . Interaction of working memory and long-term memory in the medial temporal lobe.  Cereb Cortex. Dec 2008;  18 (12) 2868-2878

Korrespondenzadresse